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      Moth resonant mechanics are tuned to wingbeat frequency and energetic demands

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          Abstract

          An insect’s wingbeat frequency is a critical determinant of its flight performance and varies by multiple orders of magnitude across Insecta. Despite potential energetic benefits for an insect that matches its wingbeat frequency to its resonant frequency, recent work has shown that moths may operate off their resonant peak. We hypothesized that across species, wingbeat frequency scales with resonance frequency to maintain favourable energetics, but with an offset in species that use frequency modulation as a means of flight control. The moth superfamily Bombycoidea is ideal for testing this hypothesis because their wingbeat frequencies vary across species by an order of magnitude, despite similar morphology and actuation. We used materials testing, high-speed videography and a model of resonant aerodynamics to determine how components of an insect’s flight apparatus (stiffness, wing inertia, muscle strain and aerodynamics) vary with wingbeat frequency. We find that the resonant frequency of a moth correlates with wingbeat frequency, but resonance curve shape (described by the Weis-Fogh number) and peak location vary within the clade in a way that corresponds to frequency-dependent biomechanical demands. Our results demonstrate that a suite of adaptations in muscle, exoskeleton and wing drive variation in resonant mechanics, reflecting potential constraints on matching wingbeat and resonant frequencies.

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          Most cited references46

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          Flexible mechanisms: the diverse roles of biological springs in vertebrate movement.

          The muscles that power vertebrate locomotion are associated with springy tissues, both within muscle and in connective tissue elements such as tendons. These springs share in common the same simple action: they stretch and store elastic strain energy when force is applied to them and recoil to release energy when force decays. Although this elastic action is simple, it serves a diverse set of functions, including metabolic energy conservation, amplification of muscle power output, attenuation of muscle power input, and rapid mechanical feedback that may aid in stability. In recent years, our understanding of the mechanisms and importance of biological springs in locomotion has advanced significantly, and it has been demonstrated that elastic mechanisms are essential for the effective function of the muscle motors that power movement. Here, we review some recent advances in our understanding of elastic mechanisms, with an emphasis on two proposed organizing principles. First, we review the evidence that the various functions of biological springs allow the locomotor system to operate beyond the bounds of intrinsic muscle properties, including metabolic and mechanical characteristics, as well as motor control processes. Second, we propose that an energy-based framework is useful for interpreting the diverse functions of series-elastic springs. In this framework, the direction and timing of the flow of energy between the body, the elastic element and the contracting muscle determine the function served by the elastic mechanism (e.g. energy conservation vs power amplification). We also review recent work demonstrating that structures such as tendons remodel more actively and behave more dynamically than previously assumed.
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            Storage of elastic strain energy in muscle and other tissues.

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              Is Open Access

              phytools 2.0: an updated R ecosystem for phylogenetic comparative methods (and other things)

              Phylogenetic comparative methods comprise the general endeavor of using an estimated phylogenetic tree (or set of trees) to make secondary inferences: about trait evolution, diversification dynamics, biogeography, community ecology, and a wide range of other phenomena or processes. Over the past ten years or so, the phytools R package has grown to become an important research tool for phylogenetic comparative analysis. phytools is a diverse contributed R library now consisting of hundreds of different functions covering a variety of methods and purposes in phylogenetic biology. As of the time of writing, phytools included functionality for fitting models of trait evolution, for reconstructing ancestral states, for studying diversification on trees, and for visualizing phylogenies, comparative data, and fitted models, as well numerous other tasks related to phylogenetic biology. Here, I describe some significant features of and recent updates to phytools, while also illustrating several popular workflows of the phytools computational software.

                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review and editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: Writing – original draftRole: Writing – review and editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – original draftRole: Writing – review and editing
                Role: Data curationRole: MethodologyRole: SoftwareRole: Writing – original draftRole: Writing – review and editing
                Role: ConceptualizationRole: MethodologyRole: Writing – original draftRole: Writing – review and editing
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review and editing
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – original draftRole: Writing – review and editing
                Journal
                Proc Biol Sci
                Proc Biol Sci
                RSPB
                royprsb
                Proceedings of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8452
                1471-2954
                June 2024
                June 26, 2024
                June 26, 2024
                : 291
                : 2025
                : 20240317
                Affiliations
                [ 1 ]School of Biological Sciences, Georgia Institute of Technology; , Atlanta, GA 30332, USA
                [ 2 ]School of Natural and Health Sciences, Seton Hill University; , Greensburg, PA 15601, USA
                [ 3 ]School of Physics, Georgia Institute of Technology; , Atlanta, GA 30332, USA
                [ 4 ]School of Electrical and Computer Engineering, Georgia Institute of Technology; , Atlanta, GA 30332, USA
                [ 5 ]Mechanical and Aerospace Engineering, University of California San Diego; , San Diego, CA 92161, USA
                Author notes

                Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.7283815.

                Author information
                https://orcid.org/0000-0002-9966-7715
                https://orcid.org/0000-0001-9034-0460
                https://orcid.org/0000-0002-9391-2476
                https://orcid.org/0000-0003-4942-4894
                Article
                rspb20240317
                10.1098/rspb.2024.0317
                11285715
                38920055
                d27f56ec-7182-4e1f-a575-579c6c58a29f
                © 2024 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : February 6, 2024
                : April 8, 2024
                : May 15, 2024
                Funding
                Funded by: Division of Integrative Organismal Systems, FundRef http://dx.doi.org/10.13039/100000154;
                Funded by: Division of Physics, FundRef http://dx.doi.org/10.13039/100000166;
                Categories
                1001
                1001
                1001
                25
                70
                Morphology & Biomechanics
                Research Articles

                Life sciences
                moth,flight,resonance,exoskeleton,wing
                Life sciences
                moth, flight, resonance, exoskeleton, wing

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